Life cycle and timing of emergence of Oligoneuriella rhenana

Ephemera, 2005 (2006), Vol. 7 (1) : 1-7
Life cycle and timing of emergence
of Oligoneuriella rhenana (IMHOFF, 1852)
in the Kyll River (SW-Germany)
[Ephemeroptera : Oligoneuriidae]
by Arne HAYBACH
Tannenweg 3, D- 55129 Mainz, E-mail : [email protected]
Keywords : Oligoneuriella rhenana, life cycle, timing of emergence, egg-laying, Germany
1) The life cycle of Oligoneuriella rhenana was studied by 2 min kick samples during the period of
occurrence of preimaginal stages. Six samples were carried out from May to August in the Kyll River
near Trier (Rhine catchment). O. rhenana is a univoltine summer species with overwintering eggs and
a single extremely fast growing generation that emerges in July and August. 2) Larvae larger than 8-10
mm were sexed, and the sex ratio was about 50:50. 3) Winged adults of O. rhenana swarming
horizontally over the water surface were collected by successive random sweeps during their daily
emergence period, and the changes in sex and stage composition were examined. 4) The emergence
occurred mainly during a 1½ h period beginning some time after sunset. Male sub-imagoes emerged
synchronously and moulted to imagoes in a 30 min period immediately prior to the emergence of
female sub-imagoes. 5) Females were mated as sub-imagoes, and the imaginal moult took place during
flight after mating, prior to egg-laying, which was done in about 3 batches. 6) Life span of winged
stages is extremely short and lasts on average about 40 min in males and about 50 min in females. 7)
Egg laying was observed to be completed in several batches, with the females leaving the turbulent
water surface several times. As the wings of Oligoneuriella remain unmoulted, the hydrophobic
quality of the subimaginal hairs is thought to be advantageous for this.
Cycle biologique et timing de l'émergence d'Oligoneuriella rhenana (Imhoff, 1852) dans la
rivière Kyll (SW de l'Allemagne) [Ephemeroptera : Oligoneuriidae]
Mot-clés : Oligoneuriella rhenana, cycle biologique, timing d'émergence, oviposition, Allemagne.
1) Le cycle biologique d'Oligoneuriella rhenana a été étudié par prélèvements foulés au pied de 2
min pendant la période d' occurrence du stade préimaginal. Six prélèvements ont été effectués de mai à
août dans la rivière Kyll près de Trier (bassin-versant du Rhin). O. rhenana est une espèce estivale
univoltine ; elle passe l'hiver à l'état d'œufs et présente une seule génération, à croissance extrêmement
rapide, qui émerge en juillet et août. 2) La détermination du sexe des larves au dessus de 8-10 mm a
révélé une sex ratio voisine de 50:50. 3) Les adultes d'O. rhenana volant en essaims horizontalement
au dessus de la surface de l'eau ont été récoltés au filet entomologique par balayages successifs au
hasard durant leur période d'émergence quotidienne, et les changements dans les proportions des sexes
et des stades subimaginal et imaginal on été examinés. 4)L'émergence a lieu principalement pendant
une période de 1 ½ h, débutant peu après le coucher du soleil. Les subimagos mâles émergent de façon
synchrone et muent en imagos sur une période de 30 minutes précédant immédiatement l'émergence
des subimagos femelles. 5) Les femelles s'accouplent au stade subimaginal, et la mue imaginale a lieu
durant le vol qui suit l'accouplement, avant l'oviposition, cette dernière se déroulant en trois fois
environ. 6) La durée de vie des stades ailés es extrêmement brève, en moyenne d'environ 40 minutes
chez les mâles et d'environ 50 minutes chez les femelles. 7) Il a été observé que l'oviposition se
2
A. HAYBACH
déroule en plusieurs fois, les femelles quittant la surface agitée de l'eau à plusieurs reprise. Du fait que
ailes d'Oligoneuriella ne s'exuvient pas, les caractéristiques hydrophobes de soies subimaginales
apparaissent comme un avantage réel.
1. Introduction
The life-cycle of Oligoneuriella rhenana has been described in general or in detail several
times as a univoltine summer cycle by several different European authors e.g. GRANDI, 1947,
PINET, 1962, SOWA, 1975, FENOGLIO et al. 2005 and others. Interestingly, little information
on its life cycle in the Rhine River, after which this species was named, has been published,
and there are only general descriptions on the time of occurrence of larvae and the flight
period e.g. in NEERACHER, 1910, SCHOENEMUND, 1930 or JANSEN, 2000. A full life cycle,
however has never been published from this area or from any other region in Germany.
The imaginal flight of Oligoneuriella rhenana has attracted early the attention of
entomologists, especially in the case of mass flights (e.g. STEINMANN, 1919 or BURMEISTER,
1989), and there are detailed descriptions on abiotic factors influencing the emergence, as
well as on flight behaviour (PINET, 1962, 1967, FISCHER, 1991, STEINMANN, 1919, GRANDI,
1947, GRIMM, 1988). However, a detailed description of the timing of emergence is missing
and this paper represents the first detailed description of the life cycle from Germany.
2. Materials and Methods
Study site
The study was conducted in the lower reach of the Kyll River at Kordel (long. 6°38' E,
lat. 39°, 45' N), a 4th-order left-handed tributary of the River Mosel near the City of Trier. The
Mosel River has its confluence with the Rhine River at Koblenz. At Kordel the river is about
10-15m wide and the water flow is very rapid and turbulent. The main substratum is stones
about 30-40 cm in diameter and pebbles. Larvae were collected about 100 m downstream,
while imagoes were collected directly above the only bridge in Kordel.
Larvae
Larvae were sampled by 2 min kick samples with a hand-net (mesh width 0,5 mm),
monthly from January to May and from September to December, and 14-daily from June to
August. Specimens of O. rhenana were preserved in 70% ethyl alcohol solution. Their lengths
without cerci were measured to the nearest 0,1 mm by use of a Wild-M3 stereo-microscope
and a measuring graticule. Starting with samples from the end of June, and with an average
size of about 8-10 mm it was possible to sex the larvae using the well-known sexual
dimorphism of the eyes as the main criterion (cf. GRANDI, 1947). Simple size-frequency
distribution was used to demonstrate the life-cycle.
Imagoes
On August, 4th 1994 a spectacular mass flight took place at the Kyll River. The time of
appearance of the swarm was noted as well as the "behaviour" of the male swarm. The
horizontal speed of the male-flight, which took place directly in front of two bridge piers, was
about 2m/s. Three years later, on August 6th, 1997 an experiment was conducted to elaborate
details on the timing of emergence in the different flight stages of Oligoneuriella largely
following the methods introduced by WATANABE et al. (1989). Soon after sunset (~ 8.00 p.m.)
the first male sub-imagoes appeared. The imagoes and sub-imagoes swarming over the water
surface were collected by random strokes through the air with an insect net of 40 cm diameter
LIFE CYCLE AND TIMING OF EMERGENCE OF OLIGONEURIELLA RHENANA
3
at a place about 3-5 m upstream of the bridge, where the water was about 30 cm deep. A tenstroke sweep was made every 10 min throughout the duration of the swarming, except for the
last 30 min, where 15 min intervals were used. The specimens of O. rhenana were preserved
in 70% ethyl alcohol solution. They were divided into their corresponding stages and sexes
using GRIMM'S (1988) features for separation: ♂-Sub-imago: tails almost as long as the body,
♂-Imago, tails longer than the body, ♀-Sub-imago: tails with distinct fringes, ♀-Imago: tails
without fringes. In addition, in female imagoes the degree of completeness of the eggs in the
abdomen was noted, because several females were observed to lay some of their eggs on the
water surface, drifting for several metres in the current, and then leaving the water again.
3. Results
Life cycle
The seasonal development of larvae in 1995 based on larval length without cerci is shown
in fig. 1. Nymphs were first collected on 15 May. Nymphs larger than 8-10 mm were
generally sexed after 29 June to estimate larval sex-ratios. No larvae were detected on April,
13th, so that, judging from the mean size of 2,65 mm in the middle of May, egg-hatching most
probably occurred between the middle and end of April in 1995. Collections on Sept. 14th
were unsuccessful, so that we can conclude that the full development from hatching to
emergence took place within approximately 3½ months.
The growth of the larvae in this species is extraordinarily fast and impressive, as has been
mentioned by several authors before. In the Kyll River Oligoneuriella larvae grow on average
between 0,2-0,3 mm per day from mid-June to the end of July. Flexible strategies are known
for O. rhenana with regard to thermal regimes (cf. FENOGLIO et al. 2005). In the Kyll River
increasing growth is correlated with increasing water temperatures and the emergence begins
at the highest water temperatures (Fig. 1), but note that only single temperature values from
the sampling dates are available.
Sex ratio and size
Last instar larvae (with black wing pads) of both sexes show size differences (Table 1).
Mature female larvae are approximately 3 mm larger than male larvae.
Sexing of larva was possible in 362 larvae: 180 were female, 182 male. There is therefore
a strong indication that the sex ratio in Oligoneuriella rhenana is about 50:50.
Date:
July 29th., 1995
Sex
♂-larva (last instar)
♀-larva (last instar)
Size (mm) :
Number of
mean ± standard deviation individuals
14,8 ± 1,0
18,1 ± 0,9
27
19
Table 1. Mean size of fullgrown larvae showing sexual dimorphism.
Tableau 1. Taille moyenne des larves en fin de développement, montrant le
dimorphisme sexuel.
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A. HAYBACH
Fig. 1 Life cycle of Oligoneuriella rhenana (Imhoff) in the River Kyll. Boxes cover all larvae within a
0,5 mm size class. Simple size frequency is shown. Black boxes indicate the occurrence of last
instar larvae, arrows indicate time of emergence. Black spots indicate water temperatures at
sampling dates (~12.00 a.m.). Numbers below the dates refer to the number of classified
specimen. Figured larva from SCHOENEMUND, 1930.
Fig. 1. Cycle biologique d'Oligoneuriella rhenana (Imhoff) dans la rivière Kyll. Les histogrammes
rendent compte de la taille de toutes les larves par classes de 0,5 mm. Les parties foncées
indiquent la présence de larves au dernier stade; les flèches indiquent la période d'émergence.
Les ponts noirs indiquent la température de l'eau aux dates de prélèvements (~ 12.00 a.m.).
Au-dessous des dates, les nombres correspondent aux spécimens classés. Figure de la larve
empruntée à Schoenemund, 1930.
LIFE CYCLE AND TIMING OF EMERGENCE OF OLIGONEURIELLA RHENANA
5
Timing of emergence
Table 2 shows the number of male sub-imagoes, male imagoes, female sub-imagoes, and
female imagoes caught by the insect net from the swarm at successive sampling times on 6
August 1997, and Fig. 2 shows the same data normalized to 100%. To estimate whether
females lay their eggs in one batch, or in several, female imagoes were separated into three
categories: First, females with complete egg packages in their abdomen, prior to egg laying.
Second, females that had partly laid their eggs, and third, females without eggs.
Central European Time p.m.
8:10 8:20 8:30 8:40 8:50 9:00 9:15 9:30
♂- Si
2
4
0
0
0
0
0
0
♂
0
14
18
14
19
1
2
0
♀- Si
0
0
0
3
0
0
0
0
♀(full with eggs)
0
0
0
0
19
10
0
0
♀ (without parts of eggs)
0
0
0
0
0
11
0
0
♀(without full of eggs)
0
0
0
0
0
0
28
12
Table 2: Timing of emergence of O. rhenana in the Kyll River on August, 6th, 1997
Tableau 2. Timing de l'émergence d'O. rhenana, rivière Kyll, le 6 août 1997.
The large majority of O. rhenana emerged synchronously within 40 min. After that time
almost only egg laying female imagoes were recorded. Male emergence began abruptly at
around 8.10 p.m. At first male sub-imagoes appeared, but the proportion of male imagoes
increased rapidly and within 20 min after detection of swarming adults, almost all males had
moulted to imagoes during swarming, as is well known for this species. After this female
sub-imagoes appeared. This stage is highly underrepresented in our data because emerging
females were rapidly mated by patrolling males and then hidden away as couples high over
the swarm. After a further 10 minutes the majority of specimens had been mated and fully
moulted female imagoes occurred to begin egg laying. Note that in O. rhenana moulting
occurs during flight, so that in adoption of this behaviour, the wings must remain unmoulted.
Within another 10 min. at 9.00 p.m. almost only female stages were captured.
Life span of adults
Individual life span may depend largely on environmental factors during flight, especially
temperature or general weather influences such as rain, storm, etc. STEINMANN (1919) reports
a 2-4 hr life span for captured individuals which had no possibility for flight. Our data based
on more natural conditions suggest that the life span of male adults is on average about 40
min, and that of female adults a little longer at about 50 min, in concordance with the field
observations of FISCHER (1991). This is one of the shortest life spans of mayflies at all, and
only Behningiidae are known to have as short or shorter life spans. In both families adults are
rapid horizontal flyers, and females are mated as subimagoes.
A. HAYBACH
6
Fig. 2. Timing of emergence of O. rhenana. Successive appearance of male-sub-imagoes, male
imagoes, female sub-imagoes, female imagoes and egg laying females is figured by use of the
data in Table 2.
Fig. 2. Timing de l'émergence d'O. rhenana. La représentation des apparitions successives des
subimagos mâles, imagos mâles, subimagoes femelles, imagos femelles, et les femelles en
oviposition est effectuée selon les données du Tableau 2.
Egg laying
O. rhenana females were observed to lay the eggs directly on the water surface, but only
in lotic areas with turbulent water and rapid flow. Females drifted 3-5 m with the current and
then left the surface to fly into the swarm again. It was not possible to observe whether they
were mated again, but this can't be excluded. Based on observations of the "degree of
emptiness" of the abdomen in the captured female imagoes, it is suggested that females lay
their eggs in at least 3 batches, and not in 1 large batch. There is perhaps some variability in
egg-laying behaviour, dependent on the size of the females, and therefore in the temperature
regime of the river in general.
4. Discussion
The current study confirmed that O. rhenana is a univoltine summer species with
overwintering eggs and a rapid, temperature dependant growth during spring and summer.
Our data also confirmed the observations and experiments of STEINMANN (1919), GRANDI
(1947) and GRIMM (1988) that female sub-imagoes of O. rhenana are mated by maleimagoes. The mating flight of this species is shown to be highly synchronic, and males appear
very shortly before females. This kind of protandry is well known for many short living mass
flyers, mainly of larger rivers, such as Dolania americana (Behningiidae: PETERS & PETERS,
1977), Ephoron virgo (Polymitarcyidae: KURECK & FONTES, 1996) or Palingenia longicauda
(Palingeniidae: RUSSEV, 1987), and is related to an optimal mating strategy in males
LIFE CYCLE AND TIMING OF EMERGENCE OF OLIGONEURIELLA RHENANA
7
(WATANABE et al., 1989). It is important to note that females lay their eggs in batches, leaving
the turbulent water surface on several occasions. For such behaviour the remaining
subimaginal haired cuticle of the wings, having hydophobic properties, is advantageous (cf.
EDMUNDS & MCCAFFERTY, 1988).
Acknowledgements
Dr. Andrea Buffagni (Brugherio) is thanked for his kind support with an Excel-program for
plotting size-frequency distributions, Prof. Dr. R. Rupprecht and Dipl.-Biol. R. Mauden (Zoological
Inst. of University of Mainz) for field assistance. Craig Macadam (Ephemeroptera Recording Scheme,
UK) is sincerely thanked for correcting the English text and for helpful comments on the manuscript.
References
BURMEISTER, E.G. 1989. Das Massenschwärmen von Flußinsekten - ein an unseren großen Flüssen
verschwundenes Phänomen. Verhandlungen des westdeutschen Entomologentags, 1988 : 59-74
EDMUNDS, G.F. JR. & W.P. MCCAFFERTY 1988. The Mayfly Subimago. Annual Review of
Entomology, 33 : 509-529.
FENOGLIO, S., BO, T., BATTEGAZZORE, M., MORISI, A. 2005. Growth of Oligoneuriella rhenana
(Imhoff, 1852) (Ephemeroptera : Oligoneuriidae) in Two Rivers with Contrasting Temperatures in
NW Italy. Zoological Studies, 44(2) : 271-274.
FISCHER, C. 1991. Evolution des Schwarmfluges und Flugverhalten der Ephemeroptera. Dissertation
Universität Erlangen, Nürnberg VI, 172 pp.
GRANDI, M. 1947. Contributi allo studio degli "Efemeroidei" italiani. IX. Oligoneuriella rhenana Imh.
Bolletino dell'Istituto di Entomologia della R. Università di Bologna, 16 : 176-218.
GRIMM, R. 1988. Zur Eintagsfliegenfauna der Donauzuflüsse Rot und Rauglen (Baden-Württemberg)
(Insecta, Ephemeroptera). Nachrichtenblatt der Bayerischen Entomologen, 37 : 73-83.
JANSEN, W. 2000. Bestandssituation der "Rheinmücke" Oligoneuriella rhenana (Imhoff, 1852)
(Ephemeroptera, Oligoneuriidae) in Deutschland. Verhandlungen des westdeutschen
Entomologentags, 1998 : 173-185.
KURECK, A., FONTES, R.J. 1996. The life cycle and emergence of Ephoron virgo, a large potamal
mayfly that has returned to the River Rhine. Archiv für Hydrobiologie, Suppl. 113 (1-4) : 319-323.
NEERACHER, F. 1910. Die Insektenfauna des Rheins und seiner Zuflüsse bei Basel. Revue Suisse de
Zoologie 18 : 497-590.
PETERS, W.L., PETERS, J.G. 1977. Adult life and emergence of Dolania americana in Northwestern
Florida (Ephemeroptera : Behningiidae). Internationale Revue der gesamten Hydrobiologie, 62 :
409-438.
PINET, J.M. 1962. Observations sur la biologie et l'ecologie d'Oligoneuriella rhenana Imhoff
(Ephemeroptera). Annales de la Station centrale d'Hydrobiologie appliquée, 9 : 303-332.
PINET, J.M. 1967. Observations sur le vol crépusculaire d'Oligoneuriella rhenana Imhoff (Ephem.
Oligoneuriidae). Bulletin de la Société Entomologique de France, 72 (5-6) : 144-155.
RUSSEV, B. 1987. Ecology, life history and distribution of Palingenia longicauda(Olivier)
(Ephemeroptera). Tijdschrift voor Entomologie, 130 : 109-127.
SCHOENEMUND, E. 1930 Eintagsfliegen oder Ephemeroptera In: Dahl (ed.) Die Tierwelt Deutschlands
und der angrenzenden Meeresgebiete, 19 : 107 pp. Fischer, Jena
SOWA, R. 1975. Ecology and biogeography of mayflies (Ephemeroptera) of running waters in the
Polish part of the Carpathians. 2. Life cycles. Acta Hydrobiologica Krakow 17(4) : 319-353.
STEINMANN, P. 1919. Zur Kenntnis der Eintagsfliege Oligoneuria rhenana. Mitteilungen der
Aargauischen Naturforschenden Gesellschaft, 15 : 58-75.
WATANABE, N.C., Yoshitaka, I., Mori, I. 1989. Timing of emergence of males and females of
Ephoron shigae (Ephemeroptera : Polymitarcyidae). Freshwater biology 21 : 473-476.
(appeared in April 2006)